1. Lindsey Horton
May 27th, 2015
The influence of prey availability on the rate of miscarriages of Southern Resident killer
whales (Orcinus orca)
Introduction
While groups of killer whales (Orcinus orca) are found in every ocean, Washington State
has a genetically unique population of killer whales in Puget Sound (Ward et al. 2009). The
population of these whales, called Southern Resident killer whales (SRKW), have declined a
staggering twenty percent starting around 1995 (Ayres et al. 2012) leading to their listing as
endangered in 2005 under the Endangered Species Act. While other areas of the world may have
different ecotypes of killer whales such as offshores and transients, (LeDuc, Robertson, and
Pitman, 2008), SRKW are a genetically distinct population which makes it important to conserve
their species and prevent extinction.
A study has attempted to identify a variety of causes that contribute to the loss of
numbers in SRKW (Ayres et al. 2012). In particular, three possible threats are of key focus
currently; noise, toxin levels, and prey availability. Noise levels from nearby boats may be a
contributor. As whale watching becomes more popular, the number of boats around San Juan
Island increases. Secondly, toxins such as PCBs (polychlorinated biphenyl) accumulate in the
blubber of killer whales because they are top predators; high toxin levels are suspected to be a
contributing factor to the decline of SRKW. Lastly, the inadequate prey hypothesis states that
their decline may be related to the small amount of Chinook salmon (Oncorhynchus
tshawytscha) available (Ayres et al. 2012). SRKW specialize in eating Chinook salmon for the
majority of their diet (Hanson et al., 2010).
2. It is important to explore possible correlations between lack of prey and miscarriage of
SRKW because if there is an association, then it may be identified as an avenue to support the
SRKW population. While there are no studies to-date of the rate of miscarriages of SRKW, there
is a study relating fecundity of SRKW to prey availability (Ward et al. 2009). There are other
variables still unknown such as how much Chinook salmon other organisms eat, including Steller
sea lions (Eumetopias jubatus) and Northern Resident killer whales (Orcinus orca). Also, it
appears that of the Chinook salmon consumed by SRKW each year, 80-90% of them are Fraser
River Chinook salmon (Ayres et al. 2012). Southern Resident Killer Whales eat up to about 12-
13% of the Fraser River Chinook Salmon population, during May to September (Williams et al.
2011).
Trying to understand consumption requirements of SRKW is the first requirement of this
study. Another important component is the current data on reproductive rates of SRKW. The rate
at which female SRKW produce calves decreases by about 50% during periods of lower Chinook
salmon availability compared to times during higher Chinook salmon availability (Ward et al.
2009). There is a strong, positive correlation between fecundity and salmon availability.
Researchers were able to find that female killer whales are sexually mature at 10 years of age
and only produce a calf every 5 years after a gestation period of 16 months (Ward et al. 2009).
The long gestation period necessitates understanding the factors that contribute to healthy
pregnancies.
This study seeks to explain how the miscarriages of SRKW are affected by prey
availability. I predict that the lack of Chinook salmon is associated with an increased risk of
SRKW having miscarriages. This may be attributed to poor nutrition. A lack of Chinook salmon
will be defined as not enough salmon to meet the established need of an individual SRKW: 410
3. to 953 typical, 4-year old Chinook salmon per day (Williams et al. 2011). Currently, while less
prey abundance is correlated with decreased fecundity in SRKW, it is not understood if less prey
abundance is correlated to miscarriages in SRKW females. If the hypothesis is correct, then these
killer whales may benefit from stricter management of Fraser River Chinook salmon stocks to
increase prey abundance.
There appears to be high salmon density around the south-west side of San Juan Island
where the whales are seen foraging in July and August (Basran, 2011). There were strong
correlations between the presence of Fraser River Chinook salmon and whale sightings in those
areas (Basran, 2011). In addition, even though Chinook salmon are the preferred prey, they are
the least abundant species of salmon in the Pacific Ocean (Ford and Ellis, 2006). This makes the
problem of prey availability a larger issue especially based on the fact that Chinook salmon also
are listed as endangered.
Another alternative hypothesis could be that the miscarriages of Southern Resident killer
whale females are associated with a mother’s increased susceptibility to disease (Robinson and
Klein, 2012). It has been found in humans that inflammatory responses that could terminate the
fetus are suppressed and instead the body increases levels of antibodies transferred to the fetus.
This leaves a pregnant female vulnerable to sickness (Robinson and Klein, 2012). Lastly, the
toxicity levels in the salmon may also contribute to increased susceptibility of disease in SRKW
(Ayres et al. 2012).
Methods
I plan to use Center for Whale Research to identify which females are most likely to
breed in the next two years, based on their known reproductive cycles. This is similar to the
method employed by Ward et al. (2009) when they used the Center for Whale Research to
4. determine birth rates. Using this data, my team will target certain females when measuring
hormone levels. As the past researchers did, I will look at data from the Pacific Salmon
Commission and Pacific Fishery Management (PSCPFM) in order to determine current salmon
population abundance rates. The PSCPFM publishes annual reports describing the current
population rates of various salmon species including Chinook salmon. The most recent report
available to the public is through their website and includes information of 2011/2012 which was
published in 2014.
Each whale is a separate case to be looked at and studied individually. The only whales
studied are the females belonging to the Southern Resident killer whale group. In total there are
three categories. The first are whales who have signs of a miscarriage and most likely had a
spontaneous abortion (also called a miscarriage). The second category are whales that have had
a successful pregnancy and birth. Lastly, the third category are the females who aren’t pregnant
but of breeding age; 10 years and above (Ward et al. 2009). It is necessary to compare the whales
who have miscarriages to healthy pregnancies and normal non-pregnant females to ensure
internal validity (West et al. 2014).
The first step is to identify the hormone used to track possible miscarriages. The hormone
free thyroxine (T4) and triiodothyronine (T3) are seen at low levels in captive bottlenose
dolphins (Tursiops) who have experienced a miscarriage. In West et al. (2014), these hormones
were compared in both successful and unsuccessful pregnancies and levels were monitored in
early, mid, and late pregnancy to understand the typical hormone levels.
One possible reason that some dolphins have low T4 and T3 levels is due to the presence
of hypothyroidism. Since bottlenose dolphins and killer whales both come from the Delphinidae
5. family, it would be logical to assume that this hormone is present in killer whales and may also
be measured to detect miscarriages.
The second step is to measure thyroid hormone levels in individuals of each of the three
categories. The hormones may be detected in scat samples. T3 is one such hormone that was
measured from Southern Resident killer whale scat. It is also associated with the amount of
Fraser River Chinook salmon consumed (Ayres et al. 2012). To obtain hormone data of SRKW
scat, I plan to collaborate with the researchers of Ayres et al. (2012) and ask to share the data
they obtained. They gathered scat samples and analyzed hormone levels from various whales of
the SRKW population in their study. It will be important to use individual identification to
separate the female whales into the three groups: those with successful births, no pregnancies
currently, and those with miscarriage indicators. To help in the identification, life history data
from the Center for Whale Research will be paired with the T3 information from Ayres et al.
(2012).
Scat has proven to be a very successful method of measuring thyroid hormones such as
T3 and T4 in mammals (Wasser et al. 2010). This method was validated partly because it was
used on a wide variety of mammals. These included African elephants and killer whales among
many other types. As aforementioned, these thyroid hormones are important predictors of
miscarriages. As Wasser et al. (2010) highlights, the method employed by Ayres et al. (2012) is a
reliable measure. The data that this new study will use from Ayres et al. (2012) will come from a
valid source.
Anticipated Results
I suspect that our study will confirm a correlation between prey availability and
miscarriages of Southern Resident killer whales. Specifically, I suspect that a lack of Chinook
6. salmon will increase the risk of miscarriages. These findings would highlight the importance of
understanding the biological and ecological needs of Chinook salmon and encourage efforts to
stabilize and increase the endangered population of the Fraser River. While the SRKW face
many other obstacles, strong evidence indicated that without significant amounts of Chinook
salmon in their diet, SRKW will not fully recover.
One master’s-level student will be hired to assist with the project for the full two years. A
graduate student is needed because there is a more data to gather than I alone can accomplish.
The graduate student will work on gathering the information on salmon densities while I gather
information on miscarriage rates. Then we will analyze the data. Lastly, this student will help
write and revise certain sections of the report. Two years of funding is necessary because killer
whales have a long gestation period and it takes more time to make observations.
In conclusion, the Southern Resident killer whales provide a crucial economic value for
the San Juan Island community (Anderson and Miller 2006). Whale watching boats are
increasing in number each year. This brings in an important source of income for the community
of the islands. If this report goes as I suspect it will, we will find an even more pressing need to
aid the Chinook salmon of the Fraser River to reach sustainable levels.
7. Budget
Item Rate Length of time Total Amount
Master's StudentTuition $5,042/Quarter 8 Quarters $40,336
Master's StudentSalary $1908/Month 24 Months $45,792
Master Student's
Benefits 20.6% of salary 24 months $9,433
PI Salary $32,000/Year 24 Months $64,000
PI Benefits 22.7% of salary 24 Months $14,528
IndirectCost 54.4% of directsubtotal $94,705
All costsof entire project $268,794
Timeline
Step ofProject Timeline
Start of project June 2016
Data collection June 2016 - December 2017
Data analysesandreport
writing
December 2017 - March
2018
Editingandrevisionsof report March-May 2018
Final submissionof findings June 2018
8. References
Andersen, M. S., & Miller, M. L. (2006). Onboard marine environmental education: Whale
watching in the San Juan Islands, Washington. Tourism in Marine Environments, 2(2),
111-118.
Ayres, K. L., Booth, R. K., Hempelmann, J. A., et al. (2012). Distinguishing the impacts of
inadequate prey and vessel traffic on an endangered killer whale (Orcinus orca)
population. PLoS One, 7(6), e36842.
Basran, C. (2011). Correlating Southern Resident Orca Sightings with Pacific Salmon Densities:
A Three Part Analysis.
Ford, J. K., & Ellis, G. M. (2006). Selective foraging by fish-eating killer whales Orcinus orca in
British Columbia. Marine Ecology Progress Series, 316, 185-199.
Hanson, M., Baird, R. W., Ford, J. K., et al. (2010). Species and stock identification of prey
consumed by endangered southern resident killer whales in their summer range.
Endangered Species Research, 11(1), 69-82.
LeDuc, R. G., Robertson, K. M., & Pitman, R. L. (2008). Mitochondrial sequence divergence
among Antarctic killer whale ecotypes is consistent with multiple species. Biology
Letters, 4(4), 426-429.
Robinson, D. P., & Klein, S. L. (2012). Pregnancy and pregnancy-associated hormones alter
immune responses and disease pathogenesis. Hormones and Behavior, 62(3), 263-271.
Ward, E. J., Holmes, E. E., & Balcomb, K. C. (2009). Quantifying the effects of prey abundance
on killer whale reproduction. Journal of Applied Ecology, 46(3), 632-640.
9. Wasser, S. K., Azkarate, J. C., Booth, R. K., et al. (2010). Non-invasive measurement of thyroid
hormone in feces of a diverse array of avian and mammalian species. General and
Comparative Endocrinology, 168(1), 1-7.
West, K. L., Ramer, J., Brown, J. L., et al. (2014). Thyroid hormone concentrations in relation to
age, sex, pregnancy, and perinatal loss in bottlenose dolphins (Tursiops truncatus).
General and Comparative Endocrinology, 197, 73-81.
Williams, R., Krkošek, M., Ashe, E., et al. (2011). Competing conservation objectives for
predators and prey: estimating killer whale prey requirements for Chinook salmon. PLoS
One, 6(11), e26738.